Title

medRxiv preprint doi: ; this version posted December 24, 2020. The copyright holder for this

preprint (which was not certified by peer review) is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity.

It is made available under a CC-BY-NC-ND 4.0 International license .

Title:

COVID-19 deaths detected in a systematic post-mortem surveillance study in Africa

Authors:

*Lawrence Mwananyanda,1,2 *Christopher J. Gill,1 William MacLeod,1 Geoffrey

Kwenda,4 Rachel Pieciak,1 Zachariah Mupila, 4 Francis Mupeta,5 Leah Forman,3

Luunga Ziko,5 Lauren Etter,1 and Donald Thea1

* Drs. Mwananyanda and Gill are Co-First Authors

Institutions:

1. Boston University School of Public Health, Department of Global Health

2. Right to Care ¨C Zambia

3. Boston University School of Public Health, Biostatistics and Epidemiology Data

Analytics Center (BEDAC)

4. University of Zambia, Department of Biomedical Sciences

5. University Teaching Hospital, Lusaka, Zambia, Division of Internal Medicine,

Infectious Diseases Section

Corresponding Author:

Christopher J Gill, MD MS

Associate Professor, Department of Global Health,

Boston University School of Public Health.

801 Massachusetts Avenue, Boston, MA 02118

cgill@bu.edu

Key Words: COVID-19, CV19, Mortality, Africa, Surveillance, Post Mortem

Patient and Public Involvement:

We did not involve patients or the public in this study.

NOTE: This preprint reports new research that has not been certified by peer review and should not be used to guide clinical practice.

medRxiv preprint doi: ; this version posted December 24, 2020. The copyright holder for this

preprint (which was not certified by peer review) is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity.

It is made available under a CC-BY-NC-ND 4.0 International license .

ABSTRACT

Objectives

Limited SARS CoV 2 testing in many African countries has constrained availability of

data on the impact of COVID-19 (CV19). To address this gap, we conducted a

systematic post-mortem surveillance study to directly measure the fatal impact of CV19

in an urban African population.

Design

We enrolled deceased individuals at the University Teaching Hospital (UTH) Morgue in

Lusaka, Zambia. We obtained nasopharyngeal swabs for testing via reversetranscriptase quantitative PCR (RT-qPCR) against the SARS-2 Coronavirus. We

stratified deaths by CV19 status, by location, age, sex, and underlying risk factors.

Setting

UTH is Zambia's largest tertiary care referral hospital and its morgue registers ~80% of

Lusaka¡¯s deaths.

Participants

Participants of all ages were enrolled if within 48 hours of death and if the next of kin or

representative provided written informed consent.

Results

We enrolled 372 participants between June and September 2020, and had PCR results

for 364 (99.5%). CV19 was detected in 70/364 (19.2%). The median age for CV19+

deaths was 48 years (IQR 36-72 years) and 70% were male. Most CV19+ deaths

(51/70, 72.8%) occurred in the community; none had been tested for CV19 antemortem.

Among the 19/70 facility deaths, six were tested antemortem. Among the 52/70 CV19

deaths with symptoms data, 44/52 had typical symptoms of CV19 (cough, fever,

shortness of breath), of whom only five were tested antemortem. We identified CV19

among seven children; only one had been tested antemortem. The proportion of CV19+

deaths increased with age, but 75.7% of CV19+ deaths were aged 750,000 cases of CV19, >20,000 deaths and a case fatality rate of 2.7%.6-8

The so-called ¡®Africa paradox¡¯ has been the focus of a number of editorials in prominent

journals9-13 proposing several explanatory theories. These include: 1) exposure to nonCV19 coronaviruses has induced cross-reactive herd immunity;14 2) the younger age

structure of African populations allows its populations to better tolerate CV19;15 3)

experience gained during the Ebola crisis allowed public health agencies across Africa

to better contain CV19;16 and 4) that certain live attenuated vaccines - Bacille Calmette

Guerin (BCG) vaccine, the oral polio vaccine and measles vaccines - engendered

robust non-specific innate immune responses that also protect against CV19.17-19

We postulate a more mundane explanation for the Africa paradox: insufficient data.

medRxiv preprint doi: ; this version posted December 24, 2020. The copyright holder for this

preprint (which was not certified by peer review) is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity.

It is made available under a CC-BY-NC-ND 4.0 International license .

Africa is the world¡¯s poorest continent. Disease surveillance is resource intense and

takes time to establish de novo, challenges that are magnified in a global health

emergency. CV19 deaths might be challenging to identify among countries with limited

resources to establish new disease surveillance systems, particularly in countries with

already high background mortality rates.

Since 2017, our team has been conducting systematic post-mortem surveillance for

respiratory pathogens among deceased infants in Lusaka, Zambia. With the onset of

the CV19 pandemic, we were able to quickly amend our study to expand surveillance to

include all age groups and to test for CV19. We present results from the first three

months of surveillance. Counter to expectations, CV19 deaths proved to be common.

METHODS

Study setting

According to the World Bank, Zambia is a poor country that ranked 117th out of 128

countries in terms of economic competitiveness in 2007.20 Its economy has been

stalled since 2015 due to falling copper prices, and with the CV19 pandemic, its

economy was predicted to contract in 2021 by 4.5%.20 Zambia¡¯s public debt burden is

60% of its gross domestic product, and over 50% of Zambians live below the poverty

line.21 The capital Lusaka has ~2 million citizens and is Zambia¡¯s largest city.22 In

Lusaka, the majority of the urban poor live in densely crowded peri-urban slums where

there are few places to avoid crowds, making it difficult to practice social spacing.

According to the study staff, masks were difficult to obtain and seldom worn by the

general Lusaka population during this time.

Overview of the ZPRIME study and its expansion to CV19 surveillance

The Zambia Pertussis RSV Infant Mortality Estimation study (ZPRIME) was launched in

August 2017 to measure the post-mortem prevalence of these two diseases among

young infants in southern Africa (Lusaka, Zambia). While Lusaka has dozens of health

facilities, few can issue the death certificates that are legally required to inter a body.

For the CV19 expansion, we concentrated our resources at the University Teaching

Hospital (UTH) morgue. UTH is the primary tertiary care referral hospital in Lusaka and

medRxiv preprint doi: ; this version posted December 24, 2020. The copyright holder for this

preprint (which was not certified by peer review) is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity.

It is made available under a CC-BY-NC-ND 4.0 International license .

registers at least 80% of deaths in the city, including those from UTH itself and from the

community.

In June 2020, we amended our protocol to expand enrollment to deceased individuals

of all ages and to add CV19 PCR testing. Other than these changes of scope,

ZPRIME¡¯s protocol did not change. Ethical oversight for ZPRIME and the CV19

expansion were provided by the Institutional Review Boards at Boston University and

the University of Zambia. Written informed consent was obtained from the deceased¡¯s

family members or representatives.

For the CV19 study expansion, we enrolled deceased individuals who either died in the

community or at a facility in Lusaka. We define ¡®facility deaths¡¯ as those that occurred

under care at UTH. All other deaths were defined as ¡®community deaths¡¯, which may

have included deaths referred to UTH from smaller facilities in Lusaka. From each

deceased individual, we tabulated sex, age, location of death (facility vs. community),

geographic location of the death within Lusaka, presenting symptoms, underlying risk

factors, and the results of antemortem CV19 PCR testing (if any).

Enrollment procedures

Enrollment occurred as next of kin came to claim the bodies of their loved ones at the

UTH morgue. Our only exclusion criterion was enrollment > 48 hours after death to

reduce the risk of false negative PCR results from degradation of viral RNA. An

abbreviated grief counselling session was offered unconditionally to the family

members. Due to the high volume of deaths, and our team¡¯s finite capacity, we only

enrolled Monday through Friday, 9AM to 5PM. During these times, we enrolled every

fifth death during July and every third death in August, with a daily cap of ~5 deaths per

day in both cases. In September, after the ZPRIME infant study ended allowing our full

team to focus on the CV19 project, we enrolled at a 1:1 ratio without a daily cap. Since

the enrollments were done prior to assessing clinical data, such as symptoms at

presentation, and prior to CV19 testing, this approach should not have introduced any

selection bias.

Presenting respiratory symptoms were solicited from informants from both facility and

community deaths. For facility deaths, additional clinical data were extracted from the

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